Gene expression in developing fibres of Upland cotton (Gossypium hirsutum L.) was massively altered by domestication

Abstract

BackgroundUnderstanding the evolutionary genetics of modern crop phenotypes has a dual relevance to evolutionary biology and crop improvement. Modern upland cotton (Gossypium hirsutum L.) was developed following thousands of years of artificial selection from a wild form, G. hirsutum var. yucatanense, which bears a shorter, sparser, layer of single-celled, ovular trichomes ('fibre'). In order to gain an insight into the nature of the developmental genetic transformations that accompanied domestication and crop improvement, we studied the transcriptomes of cotton fibres from wild and domesticated accessions over a developmental time course.ResultsFibre cells were harvested between 2 and 25 days post-anthesis and encompassed the primary and secondary wall synthesis stages. Using amplified messenger RNA and a custom microarray platform designed to interrogate expression for 40,430 genes, we determined global patterns of expression during fibre development. The fibre transcriptome of domesticated cotton is far more dynamic than that of wild cotton, with over twice as many genes being differentially expressed during development (12,626 versus 5273). Remarkably, a total of 9465 genes were diagnosed as differentially expressed between wild and domesticated fibres when summed across five key developmental time points. Human selection during the initial domestication and subsequent crop improvement has resulted in a biased upregulation of components of the transcriptional network that are important for agronomically advanced fibre, especially in the early stages of development. About 15% of the differentially expressed genes in wild versus domesticated cotton fibre have no homology to the genes in databases.ConclusionsWe show that artificial selection during crop domestication can radically alter the transcriptional developmental network of even a single-celled structure, affecting nearly a quarter of the genes in the genome. Gene expression during fibre development within accessions and expression alteration arising from evolutionary change appears to be 'modular' - complex genic networks have been simultaneously and similarly transformed, in a coordinated fashion, as a consequence of human-mediated selection. These results highlight the complex alteration of the global gene expression machinery that resulted from human selection for a longer, stronger and finer fibre, as well as other aspects of fibre physiology that were not consciously selected. We illustrate how the data can be mined for genes that were unwittingly targeted by aboriginal and/or modern domesticators during crop improvement and/or which potentially control the improved qualities of domesticated cotton fibre.See Commentary: http://www.biomedcentral.com/1741-7007/8/137

Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton ( Gossypium )

“…As a specialized unicellular trichome with a greatly exaggerated length, cotton fiber represents a masterpiece of human domestication, made all the more remarkable by its parallel, independent origin in four cultivated species (three studied here). Little is known about the genetic, genomic, or metabolomic transformations that mediate these independent transformations, although insights are emerging from comparative expression profiling experiments (3)(4)(5)(6). The present study sheds light on one aspect of this general question, implicating the up-regulation of the profilin gene family concomitant with strong directional selection under human domestication.…”

“…In previous investigations of cotton domestication based on microarray data, profilin genes ranked among the most highly differentially expressed genes (4,14,30), suggesting that they, or one or more upstream regulators, were targets of human selection. Moreover, this observation was repeated for three different, independently domesticated cotton species.…”

“…With respect to the former, analyses of fiber growth curves reveal that cotton domestication at both the diploid and allopolyploid levels is associated with a prolonged period of fiber elongation (2). As to the genomic underpinnings of fiber evolution, a number of recent studies are generating insights and a rich data set based on comparative transcriptome profiling of fiber development in wild vs. domesticated cotton (3)(4)(5)(6), and from ongoing comparative proteomic analyses (7). Rapp et al (2010), for example, reported thousands of genes that are differentially expressed in developing fiber between wild and domesticated G. hirsutum, many associated with key developmental processes presumed to play important roles in primary and secondary wall synthesis and in modulation of reactive oxygen species (3,5,6).…”

“…As to the genomic underpinnings of fiber evolution, a number of recent studies are generating insights and a rich data set based on comparative transcriptome profiling of fiber development in wild vs. domesticated cotton (3)(4)(5)(6), and from ongoing comparative proteomic analyses (7). Rapp et al (2010), for example, reported thousands of genes that are differentially expressed in developing fiber between wild and domesticated G. hirsutum, many associated with key developmental processes presumed to play important roles in primary and secondary wall synthesis and in modulation of reactive oxygen species (3,5,6). Thus, the evolutionary process associated with strong directional selection practiced by aboriginal domesticators appears to be extraordinarily complex, at least insofar as perturbation of the transcriptional network, especially in the early stages of fiber development (4).…”

A Genetic and Metabolic Analysis Revealed that Cotton Fiber Cell Development Was Retarded by Flavonoid Naringenin

“…In the past decade, large amounts of "omics" data about fiber development have been accumulated, and many critical developmental pathways were revealed (Ji et al, 2003;Ruan et al, 2003;Arpat et al, 2004;Shi et al, 2006;Wu et al, 2006;Hovav et al, 2008a). Flavonoid genes were widely detected in most of these data, which included all the studied cotton species (Arpat et al, 2004;Gou et al, 2007;Hovav et al, 2008b;Al-Ghazi et al, 2009;Rapp et al, 2010). In a comparison of the fiber development of Xuzhou142 and its fiberless mutant, flavonoid genes were found to be preferentially expressed in fiber cells over ovules (Gou et al, 2007).…”